Effect of fertilization regimes on continuous cropping growth constraints in watermelon is associated with abundance of key ecological clusters in the rhizosphere

https://doi.org/10.1016/j.agee.2022.108135Get rights and content

Highlights

  • Chemical fertilization aggravates watermelon continuous-cropping obstacle.

  • Organic and bio-organic fertilization alleviates continuous cropping obstacles.

  • Watermelon growth is associated with the key ecological clusters in rhizosphere.

  • Chemical fertilization inhibits the growth of beneficial bacterial taxa.

  • Organic and bio-organic fertilization inhibits the growth of pathogenic fungal taxa.

Abstract

The deterioration of the microbiome within the rhizosphere is the main reason behind continuous cropping obstacles and is affected by fertilization regimes. However, the potential associations among fertilization regimes, rhizosphere microbial communities, and the severity of continuous cropping obstacles are poorly understood. Here, we investigated how three-year fertilization regimes (including no fertilizer, chemical fertilizer, organic fertilizer, combination of chemical and organic fertilizer, and bio-organic fertilizer application) affect the rhizosphere microbiome and its associations with continuous cropping growth constraints during the whole growing period of watermelon, using a rhizobox system under greenhouse conditions. The results showed that different fertilization treatments induced drastic shifts in the richness, structure, and composition of rhizosphere microbial communities, whereas the growth stages induced few changes. Compared with no fertilizer treatment, the continuous application of chemical fertilizer inhibited the growth of watermelon. This was strongly associated with the reduced abundance of key ecological clusters within the bacterial co-occurrence network, which contains beneficial bacterial taxa, such as Lysobacter sp. and Haliangium sp. In contrast, continuous application of organic and bio-organic fertilizers promoted the growth of watermelon and was associated with the decreased abundance of key ecological clusters within the fungal co-occurrence network, which contains pathogenic fungal taxa, such as Fusarium sp., Cladosporium sp., and Acremonium sp. Overall, continuous chemical fertilizer application can induce severe continuous cropping obstacles by inhibiting the growth of beneficial bacteria. Continuous application of organic and bio-organic fertilizers can help alleviate such obstacles by suppressing pathogenic fungi. These findings reveal the microbial mechanisms underlying the effects of different fertilization regimes on continuous cropping growth constraints of watermelon.

Introduction

Continuous cropping obstacle refers to the suppressed growth of crops following long-term planting of the same crop variety on the same land (Wang et al., 2020, Wang et al., 2020). In China, owing to the high production requirements and limited availability of arable areas, the same crop is usually grown in the same land continuously without interruption (Chen et al., 2018, Chen et al., 2018). Large areas of croplands and greenhouses are threatened by continuous cropping obstacle, which causes severe soil-borne diseases and suppresses plant growth (Li et al., 2019). There are many explanations for these problems, including decreased soil fertility, nutrient depletion, biodiversity loss, soil acidification, salinity, compaction, accumulation of autotoxic chemicals, buildup of soil-borne pathogens, and reduced abundance of plant growth-promoting microbes (Aparicio and Costa, 2007, Chen et al., 2012, Nayyar et al., 2009). Among them, deterioration of the soil microbial community, particularly within the rhizosphere of plants, is the main reason for this phenomenon (Chen et al., 2018, Chen et al., 2018). The rhizosphere microbiome is crucial for disease suppression and is closely related to plant growth and soil health (de Faria et al., 2020, Qu et al., 2020, Xue and Wang, 2020). In the rhizosphere, harmful microbes interact with other microbial taxa in the rhizosphere microbial communities, and these interactions determine whether plants would be infected and their growth would be suppressed (Chaparro et al., 2012, Semenov et al., 2020). Therefore, identifying the changes in microbial communities within the rhizosphere of plants may help reveal the causes of continuous cropping obstacles and provide insights for preventing them through rhizosphere engineering.

Watermelon (Citrullus lanatus) is an important cucurbit crop, which is favored by farmers owing to its high economic benefit and nutrient value (Ding et al., 2021). However, watermelon crops, particularly under continuous long-term monoculture, can develop continuous cropping obstacle, with severe soil-borne diseases, high seedling mortality, stunted plant growth, and declined plant vigor, resulting in low fruit yield and quality and massive economic losses (Ling et al., 2014). Fertilization is essential in watermelon production to meet the nutritional needs of plants. However, various fertilization regimes have differing influences on the rhizosphere microbial assembly and may either aggravate or alleviate continuous cropping obstacles. For example, in a peanut (Arachis hypogaea L.) monoculture system, researchers found that the application of organic fertilizers, compared with chemical fertilizers, better optimized the rhizobacteria and decreased the abundance of bacterial wilt pathogen (Ralstonia), resulting in a significant decline in bacterial wilt disease and higher kernel yields of peanut, after 20 years of continuous cropping (Chen et al., 2018, Chen et al., 2018). Reduced application of chemical fertilizers was reported to mitigate continuous cropping obstacles in a cucumber production system, as the abundance of Pseudomonas, which defends against possible fungal pathogens, increased significantly in the rhizosphere (Fu et al., 2020). Moreover, the application of bio-organic fertilizer was reported to minimally alter bacterial diversity and enhance the recruitment of beneficial bacteria, which effectively mitigated the continuous cropping obstacles and suppressed Fusarium wilt of watermelon (Ling et al., 2014). However, there remains a lack of comprehensive comparison of the effects of various fertilization regimes on rhizosphere microbial communities after continuous cropping. The potential associations among fertilization regimes, rhizosphere microbial communities, and the severity of continuous cropping obstacles of watermelon remain poorly understood.

Therefore, in the present study, we aimed to: (1) investigate the effects of different fertilization regimes on the rhizosphere microbial communities during the whole growth period of watermelon after three years of continuous cultivation, and (2) demonstrate the potential associations between the growth of watermelon plant and the composition of the rhizosphere microbiome, which is affected by fertilization regimes. To this end, we used a rhizobox system that enabled nondestructive repeated sampling of individual watermelon plants treated with various fertilization regimes during the growth period under greenhouse conditions. Microbial communities in the rhizosphere soils across five watermelon plant growth stages (seedling, branching, flowering, fruiting, and maturity stages) under different fertilization treatments (no fertilizer, chemical fertilizer, organic fertilizer, combined use of chemical and organic fertilizers, and bio-organic fertilizer) after three years of continuous cultivation were detected, and the potential correlation between microbial communities within the rhizosphere and the growth of watermelon was deduced. These results would provide insights into the micro-ecological mechanism underlying the effect of different fertilization treatments on the severity of continuous cropping obstacles, thereby providing a theoretical basis for the control of continuous cropping obstacles and maintaining soil health through regulating rhizosphere microbiota in the agricultural system (Kuzyakov et al., 2020, Zhang et al., 2020).

Section snippets

Field site

The field experiment site was located in Zhuanghang Experimental Station of Shanghai Academy of Agricultural Sciences, Shanghai, China (30° 53' 419" N, 121°23' 158" E). This region has a subtropical maritime monsoon climate, with a mean precipitation of 1221.4 mm and temperature of 15.6 °C. The soil in this site is classified as Eutric Cambisols according to the FAO classification. The basic properties of the upper layer soil (0–20 cm) in the field prior to the experiment were as follows: soil

Growth of watermelon plants

After three years of continuous cultivation, watermelon biomass was observed to be the highest under the BOF treatment followed by the OF treatment, while the lowest biomass was observed under the CF treatment (Fig. 1). The growth of watermelon was suppressed by 16.5 % under the CF treatment compared with the CK treatment, but improved by 33.1–59.2 % due to the application of OF and BOF. MF treatment slightly decreased the biomass of watermelon compared with the CK treatment, but not

Effect of different fertilization regimes on the growth of watermelon after continuous cultivation

After comparing the effects of different fertilization regimes on the growth of watermelon upon three years continuous cultivation, we found that the application of bio-organic and organic fertilizers increased, while the application of chemical fertilizers decreased the biomass of watermelon, compared with the results from the control group. Combined application of chemical and organic fertilizers exerted less noticeable effects on the biomass of watermelon. These results indicate that organic

Conclusions

Overall, our results suggest that the continuous cropping growth constraints in the case of watermelon are aggravated by CF but alleviated by OF and BOF. This effect is associated with the abundance of key ecological clusters in the rhizosphere soil across all the growing stages of watermelon. The application of chemical fertilizers inhibited the growth of keystone beneficial bacterial taxa. In contrast, the application of organic and bio-organic fertilizers inhibited the growth of keystone

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

This study was financially supported by Ningbo Science and Technology Bureau (2021Z047; 2021Z04), the Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan) (CUG170104), Department of Agriculture and Rural Development of Zhejiang Province (2022SNJF024), The SAAS Program for Excellent Research Team (Nong Ke Zhuo 2022(008)), Science and Technology Commission of Shanghai Municipality (19DZ1204705), National Agricultural Experimental Station for

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